Evolutionary dynamics in the Anthropocene: Life history and intensity of human contact shape antipredator responses

Type Article
Date 2020-09
Language English
Author(s) Geffroy Benjamin1, Sadoul Bastien1, Putman Breanna J.2, Berger-Tal Oded3, Garamszegi László Zsolt4, Møller Anders Pape5, 6, Blumstein Daniel T.2, de Waal Frans B. M.
Affiliation(s) 1 : MARBEC, Univ Montpellier, Ifremer, IRD, CNRS, Palavas-Les-Flots, France
2 : Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, United States of America, Natural History Museum of Los Angeles County, Department of Herpetology and Urban Nature Research Center, Los Angeles, California, United States of America
3 : Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Israel
4 : Centre for Ecological Research, Institute of Ecology and Botany, Vácrátót, Hungary, MTA-ELTE, Theoretical Biology and Evolutionary Ecology Research Group, Department of Plant Systematics, Ecology and Theoretical Biology, Eötvös Loránd University, Budapest, Hungary
5 : Laboratoire d’Ecologie, Systematique et Evolution, Centre National de la Recherche Scientifique, Universite Paris-Sud, France
6 : Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, China
Source Plos Biology (1544-9173) (Public Library of Science (PLoS)), 2020-09 , Vol. 18 , N. 9 , P. e3000818 (17p.)
DOI 10.1371/journal.pbio.3000818
WOS© Times Cited 30

Humans profoundly impact landscapes, ecosystems, and animal behavior. In many cases, animals living near humans become tolerant of them and reduce antipredator responses. Yet, we still lack an understanding of the underlying evolutionary dynamics behind these shifts in traits that affect animal survival. Here, we used a phylogenetic meta-analysis to determine how the mean and variability in antipredator responses change as a function of the number of generations spent in contact with humans under 3 different contexts: urbanization, captivity, and domestication. We found that any contact with humans leads to a rapid reduction in mean antipredator responses as expected. Notably, the variance among individuals over time observed a short-term increase followed by a gradual decrease, significant for domesticated animals. This implies that intense human contact immediately releases animals from predation pressure and then imposes strong anthropogenic selection on traits. In addition, our results reveal that the loss of antipredator traits due to urbanization is similar to that of domestication but occurs 3 times more slowly. Furthermore, the rapid disappearance of antipredator traits was associated with 2 main life-history traits: foraging guild and whether the species was solitary or gregarious (i.e., group-living). For domesticated animals, this decrease in antipredator behavior was stronger for herbivores than for omnivores or carnivores and for solitary than for gregarious species. By contrast, the decrease in antipredator traits was stronger for gregarious, urbanized species, although this result is based mostly on birds. Our study offers 2 major insights on evolution in the Anthropocene: (1) changes in traits occur rapidly even under unintentional human “interventions” (i.e., urbanization) and (2) there are similarities between the selection pressures exerted by domestication and by urbanization. In all, such changes could affect animal survival in a predator-rich world, but through understanding evolutionary dynamics, we can better predict when and how exposure to humans modify these fitness-related traits.

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Publisher's official version 17 1 MB Open access
S1 PRISMA Checklist. PRISMA flow diagram describing literature search, selection, and analyses. 954 KB Open access
S1 Fig. Derivatives of changes observed over generations for the mean of antipredator traits in the 3 contexts of human presence. 185 KB Open access
S2 Fig. The decrease in average antipredator traits over generations of domestication differs as a function of animal’s taxon. 243 KB Open access
S3 Fig. Origin of the data used for the meta-analysis. 2 MB Open access
S4 Fig. Phylogenetic trees of animals used in the phylogenetic meta-analysis for (A) domesticated, (B) captive, and (C) urbanized species. All data and R code supporting the figure are available in.. 2 MB Open access
S1 Table. Meta-analytic estimates of the slopes (fitted using MCMCglmm) of factors that best describe how generation time affects normalized-mean and CV of antipredator ... 9 KB Open access
S2 Table. Comparison of the models presenting all combinations of life-history traits “foraging guild,” “social level,” and “longevity maximum” for urbanized and domesticated contexts. 9 KB Open access
S3 Table. Meta-analytic estimates of the intercept and slopes (fitted using MCMCglmm) of factors that best describe how generation time affects normalized-mean of ... 10 KB Open access
S4 Table. The different antipredator traits investigated in our study. 5 KB Open access
S5 Table. Life-history traits of the species used in the analyses. 62 KB Open access
S6 Table. Estimates of heterogeneity I2 (%) from the normalized-mean meta-analysis and the CV meta-analysis for the best model with all random factors for the 3 different ... 11 KB Open access
S1 Data. All data for the meta-analysis, (A) initial data management, (B) data management, and (C) R code and data. 1 MB Open access
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How to cite 

Geffroy Benjamin, Sadoul Bastien, Putman Breanna J., Berger-Tal Oded, Garamszegi László Zsolt, Møller Anders Pape, Blumstein Daniel T., de Waal Frans B. M. (2020). Evolutionary dynamics in the Anthropocene: Life history and intensity of human contact shape antipredator responses. Plos Biology, 18(9), e3000818 (17p.). Publisher's official version : https://doi.org/10.1371/journal.pbio.3000818 , Open Access version : https://archimer.ifremer.fr/doc/00652/76397/